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      Climate-driven declines in arthropod abundance restructure a rainforest food web

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          Significance

          Arthropods, invertebrates including insects that have external skeletons, are declining at an alarming rate. While the tropics harbor the majority of arthropod species, little is known about trends in their abundance. We compared arthropod biomass in Puerto Rico’s Luquillo rainforest with data taken during the 1970s and found that biomass had fallen 10 to 60 times. Our analyses revealed synchronous declines in the lizards, frogs, and birds that eat arthropods. Over the past 30 years, forest temperatures have risen 2.0 °C, and our study indicates that climate warming is the driving force behind the collapse of the forest’s food web. If supported by further research, the impact of climate change on tropical ecosystems may be much greater than currently anticipated.

          Abstract

          A number of studies indicate that tropical arthropods should be particularly vulnerable to climate warming. If these predictions are realized, climate warming may have a more profound impact on the functioning and diversity of tropical forests than currently anticipated. Although arthropods comprise over two-thirds of terrestrial species, information on their abundance and extinction rates in tropical habitats is severely limited. Here we analyze data on arthropod and insectivore abundances taken between 1976 and 2012 at two midelevation habitats in Puerto Rico’s Luquillo rainforest. During this time, mean maximum temperatures have risen by 2.0 °C. Using the same study area and methods employed by Lister in the 1970s, we discovered that the dry weight biomass of arthropods captured in sweep samples had declined 4 to 8 times, and 30 to 60 times in sticky traps. Analysis of long-term data on canopy arthropods and walking sticks taken as part of the Luquillo Long-Term Ecological Research program revealed sustained declines in abundance over two decades, as well as negative regressions of abundance on mean maximum temperatures. We also document parallel decreases in Luquillo’s insectivorous lizards, frogs, and birds. While El Niño/Southern Oscillation influences the abundance of forest arthropods, climate warming is the major driver of reductions in arthropod abundance, indirectly precipitating a bottom-up trophic cascade and consequent collapse of the forest food web.

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          Most cited references118

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          Modeled impact of anthropogenic warming on the frequency of intense Atlantic hurricanes.

          Several recent models suggest that the frequency of Atlantic tropical cyclones could decrease as the climate warms. However, these models are unable to reproduce storms of category 3 or higher intensity. We explored the influence of future global warming on Atlantic hurricanes with a downscaling strategy by using an operational hurricane-prediction model that produces a realistic distribution of intense hurricane activity for present-day conditions. The model projects nearly a doubling of the frequency of category 4 and 5 storms by the end of the 21st century, despite a decrease in the overall frequency of tropical cyclones, when the downscaling is based on the ensemble mean of 18 global climate-change projections. The largest increase is projected to occur in the Western Atlantic, north of 20 degrees N.
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            Why tropical forest lizards are vulnerable to climate warming.

            Biological impacts of climate warming are predicted to increase with latitude, paralleling increases in warming. However, the magnitude of impacts depends not only on the degree of warming but also on the number of species at risk, their physiological sensitivity to warming and their options for behavioural and physiological compensation. Lizards are useful for evaluating risks of warming because their thermal biology is well studied. We conducted macrophysiological analyses of diurnal lizards from diverse latitudes plus focal species analyses of Puerto Rican Anolis and Sphaerodactyus. Although tropical lowland lizards live in environments that are warm all year, macrophysiological analyses indicate that some tropical lineages (thermoconformers that live in forests) are active at low body temperature and are intolerant of warm temperatures. Focal species analyses show that some tropical forest lizards were already experiencing stressful body temperatures in summer when studied several decades ago. Simulations suggest that warming will not only further depress their physiological performance in summer, but will also enable warm-adapted, open-habitat competitors and predators to invade forests. Forest lizards are key components of tropical ecosystems, but appear vulnerable to the cascading physiological and ecological effects of climate warming, even though rates of tropical warming may be relatively low.
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              Comparative losses of British butterflies, birds, and plants and the global extinction crisis.

              There is growing concern about increased population, regional, and global extinctions of species. A key question is whether extinction rates for one group of organisms are representative of other taxa. We present a comparison at the national scale of population and regional extinctions of birds, butterflies, and vascular plants from Britain in recent decades. Butterflies experienced the greatest net losses, disappearing on average from 13% of their previously occupied 10-kilometer squares. If insects elsewhere in the world are similarly sensitive, the known global extinction rates of vertebrate and plant species have an unrecorded parallel among the invertebrates, strengthening the hypothesis that the natural world is experiencing the sixth major extinction event in its history.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                30 October 2018
                15 October 2018
                15 October 2018
                : 115
                : 44
                : E10397-E10406
                Affiliations
                [1] aDepartment of Biological Sciences, Rensselaer Polytechnic University , Troy, NY 12180;
                [2] bEstación de Biología Chamela, Instituto de Biología, Universidad Nacional Autónoma de México , 47152 Chamela, Jalisco, Mexico
                Author notes
                1To whom correspondence should be addressed. Email: listeb@ 123456rpi.edu .

                Edited by Nils Christian Stenseth, University of Oslo, Oslo, Norway, and approved September 10, 2018 (received for review January 8, 2018)

                Author contributions: B.C.L. and A.G. designed research; B.C.L. and A.G. performed research; B.C.L. and A.G. analyzed data; and B.C.L. wrote the paper.

                Article
                201722477
                10.1073/pnas.1722477115
                6217376
                30322922
                834d0a36-19c6-4972-bf56-a01d5863be57
                Copyright © 2018 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 10
                Funding
                Funded by: NSF
                Award ID: 1038013
                Award Recipient : Bradford C Lister
                Categories
                PNAS Plus
                Biological Sciences
                Ecology
                PNAS Plus

                climate warming,rainforest,food web,arthropods,bottom-up cascade

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